NOTCH2 participates in Jagged1-induced osteogenic differentiation in human periodontal ligament cells.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
07 08 2020
07 08 2020
Historique:
received:
16
04
2020
accepted:
27
07
2020
entrez:
10
8
2020
pubmed:
10
8
2020
medline:
17
12
2020
Statut:
epublish
Résumé
Jagged1 activates Notch signaling and subsequently promotes osteogenic differentiation in human periodontal ligament cells (hPDLs). The present study investigated the participation of the Notch receptor, NOTCH2, in the Jagged1-induced osteogenic differentiation in hPDLs. NOTCH2 and NOTCH4 mRNA expression levels increased during hPDL osteogenic differentiation. However, the endogenous NOTCH2 expression levels were markedly higher compared with NOTCH4. NOTCH2 expression knockdown using shRNA in hPDLs did not dramatically alter their proliferation or osteogenic differentiation compared with the shRNA control. After seeding on Jagged1-immobilized surfaces and maintaining the hPDLs in osteogenic medium, HES1 and HEY1 mRNA levels were markedly reduced in the shNOTCH2-transduced cells compared with the shControl group. Further, shNOTCH2-transduced cells exhibited less alkaline phosphatase enzymatic activity and in vitro mineralization than the shControl cells when exposed to Jagged1. MSX2 and COL1A1 mRNA expression after Jagged1 activation were reduced in shNOTCH2-transduced cells. Endogenous Notch signaling inhibition using a γ-secretase inhibitor (DAPT) attenuated mineralization in hPDLs. DAPT treatment significantly promoted TWIST1, but decreased ALP, mRNA expression, compared with the control. In conclusion, Notch signaling is involved in hPDL osteogenic differentiation. Moreover, NOTCH2 participates in the mechanism by which Jagged1 induced osteogenic differentiation in hPDLs.
Identifiants
pubmed: 32770090
doi: 10.1038/s41598-020-70277-7
pii: 10.1038/s41598-020-70277-7
pmc: PMC7414879
doi:
Substances chimiques
JAG1 protein, human
0
Jagged-1 Protein
0
NOTCH2 protein, human
0
RNA, Messenger
0
Receptor, Notch2
0
Receptors, Notch
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
13329Références
Canalis, E. et al. Notch signaling in osteocytes differentially regulates cancellous and cortical bone remodeling. J. Biol. Chem.288, 25614–25625 (2013).
doi: 10.1074/jbc.M113.470492
Regan, J. & Long, F. Notch signaling and bone remodeling. Curr. Osteoporos. Rep.11, 126–129 (2013).
doi: 10.1007/s11914-013-0145-4
Kikuta, J., Yamaguchi, M., Shimizu, M., Yoshino, T. & Kasai, K. Notch signaling induces root resorption via RANKL and IL-6 from hPDL cells. J. Dent. Res.94, 140–147 (2015).
doi: 10.1177/0022034514555364
Manokawinchoke, J., Sumrejkanchanakij, P., Subbalekha, K., Pavasant, P. & Osathanon, T. Jagged1 inhibits osteoprotegerin expression by human periodontal ligament cells. J. Periodontal. Res.51, 789–799 (2016).
doi: 10.1111/jre.12357
Nakao, A. et al. PTHrP induces Notch signaling in periodontal ligament cells. J. Dent. Res.88, 551–556 (2009).
doi: 10.1177/0022034509337899
Tanabe, H. et al. Periostin associates with Notch1 precursor to maintain Notch1 expression under a stress condition in mouse cells. PLoS ONE5, e12234 (2010).
doi: 10.1371/journal.pone.0012234
Osathanon, T., Nowwarote, N., Manokawinchoke, J. & Pavasant, P. bFGF and JAGGED1 regulate alkaline phosphatase expression and mineralization in dental tissue-derived mesenchymal stem cells. J. Cell Biochem.114, 2551–2561 (2013).
doi: 10.1002/jcb.24602
Osathanon, T. et al. Surface-bound orientated Jagged-1 enhances osteogenic differentiation of human periodontal ligament-derived mesenchymal stem cells. J. Biomed. Mater. Res. A101, 358–367 (2013).
doi: 10.1002/jbm.a.34332
Liu, L., Ling, J., Wei, X., Wu, L. & Xiao, Y. Stem cell regulatory gene expression in human adult dental pulp and periodontal ligament cells undergoing odontogenic/osteogenic differentiation. J. Endod.35, 1368–1376 (2009).
doi: 10.1016/j.joen.2009.07.005
Li, Y., Li, S. Q., Gao, Y. M., Li, J. & Zhang, B. Crucial role of Notch signaling in osteogenic differentiation of periodontal ligament stem cells in osteoporotic rats. Cell Biol. Int.38, 729–736 (2014).
doi: 10.1002/cbin.10257
Hozumi, K. Distinctive properties of the interactions between Notch and Notch ligands. Dev. Growth Differ.62, 49–58 (2020).
doi: 10.1111/dgd.12641
Mitsiadis, T. A., Lardelli, M., Lendahl, U. & Thesleff, I. Expression of Notch 1, 2 and 3 is regulated by epithelial-mesenchymal interactions and retinoic acid in the developing mouse tooth and associated with determination of ameloblast cell fate. J. Cell Biol.130, 407–418 (1995).
doi: 10.1083/jcb.130.2.407
Meester, J. A. N. et al. Overlapping but distinct roles for NOTCH receptors in human cardiovascular disease. Clin. Genet.95, 85–94 (2019).
doi: 10.1111/cge.13382
Nowwarote, N. et al. Characterization of a bioactive Jagged1-coated polycaprolactone-based membrane for guided tissue regeneration. Arch. Oral Biol.88, 24–33 (2018).
doi: 10.1016/j.archoralbio.2018.01.007
Zhu, F., Sweetwyne, M. T. & Hankenson, K. D. PKCdelta is required for Jagged-1 induction of human mesenchymal stem cell osteogenic differentiation. Stem Cells31, 1181–1192 (2013).
doi: 10.1002/stem.1353
Osathanon, T. et al. Notch signaling is involved in neurogenic commitment of human periodontal ligament-derived mesenchymal stem cells. Stem Cells Dev.22, 1220–1231 (2013).
doi: 10.1089/scd.2012.0430
Hansamuit, K., Osathanon, T. & Suwanwela, J. Effect of Jagged1 on the expression of genes in regulation of osteoblast differentiation and bone mineralization ontology in human dental pulp and periodontal ligament cells. J. Oral Biol. Craniofac. Res.10, 233–237 (2020).
doi: 10.1016/j.jobcr.2019.12.003
Osathanon, T. et al. Jagged1 promotes mineralization in human bone-derived cells. Arch. Oral Biol.99, 134–140 (2019).
doi: 10.1016/j.archoralbio.2019.01.013
Manokawinchoke, J. et al. Indirect immobilized Jagged1 suppresses cell cycle progression and induces odonto/osteogenic differentiation in human dental pulp cells. Sci. Rep.7, 10124 (2017).
doi: 10.1038/s41598-017-10638-x
Dishowitz, M. I. et al. Jagged1 immobilization to an osteoconductive polymer activates the Notch signaling pathway and induces osteogenesis. J. Biomed. Mater. Res. A102, 1558–1567 (2014).
doi: 10.1002/jbm.a.34825
Osathanon, T., Manokawinchoke, J., Egusa, H. & Pavasant, P. Notch signaling partly regulates the osteogenic differentiation of retinoic acid-treated murine induced pluripotent stem cells. J. Oral. Sci.59, 405–413 (2017).
doi: 10.2334/josnusd.16-0552
Shimizu, T. et al. Notch signaling induces osteogenic differentiation and mineralization of vascular smooth muscle cells: role of Msx2 gene induction via Notch-RBP-Jk signaling. Arterioscler. Thromb. Vasc. Biol.29, 1104–1111 (2009).
doi: 10.1161/ATVBAHA.109.187856
Anant, S., Roy, S. & VijayRaghavan, K. Twist and Notch negatively regulate adult muscle differentiation in Drosophila. Development125, 1361–1369 (1998).
pubmed: 9502718
Zhang, X. W. et al. Twist-related protein 1 negatively regulated osteoblastic transdifferentiation of human aortic valve interstitial cells by directly inhibiting runt-related transcription factor 2. J. Thorac. Cardiovasc. Surg.148, 1700–1708 (2014).
doi: 10.1016/j.jtcvs.2014.02.084
Komaki, M. et al. Twist negatively regulates osteoblastic differentiation in human periodontal ligament cells. J. Cell. Biochem.100, 303–314 (2007).
doi: 10.1002/jcb.21038
Manokawinchoke, J., Sumrejkanchanakij, P., Pavasant, P. & Osathanon, T. Notch signaling participates in TGF-beta-induced SOST expression under intermittent compressive stress. J. Cell Physiol.232, 2221–2230 (2017).
doi: 10.1002/jcp.25740
Baeten, J. T. & Lilly, B. Differential regulation of NOTCH2 and NOTCH3 contribute to their unique functions in vascular smooth muscle cells. J. Biol. Chem.290, 16226–16237 (2015).
doi: 10.1074/jbc.M115.655548
Baumgart, A. et al. Opposing role of Notch1 and Notch2 in a Kras(G12D)-driven murine non-small cell lung cancer model. Oncogene34, 578–588 (2015).
doi: 10.1038/onc.2013.592
Yorgan, T. et al. Osteoblast-specific Notch2 inactivation causes increased trabecular bone mass at specific sites of the appendicular skeleton. Bone87, 136–146 (2016).
doi: 10.1016/j.bone.2016.04.012
Ongaro, A. et al. Characterization of notch signaling during osteogenic differentiation in human osteosarcoma cell line MG63. J. Cell Physiol.231, 2652–2663 (2016).
doi: 10.1002/jcp.25366
Chakravorty, N. et al. Pro-osteogenic topographical cues promote early activation of osteoprogenitor differentiation via enhanced TGFbeta, Wnt, and Notch signaling. Clin. Oral Implants Res.25, 475–486 (2014).
doi: 10.1111/clr.12178
Hoac, B., Nelea, V., Jiang, W., Kaartinen, M. T. & McKee, M. D. Mineralization-inhibiting effects of transglutaminase-crosslinked polymeric osteopontin. Bone101, 37–48 (2017).
doi: 10.1016/j.bone.2017.04.007
Livak, K. J. & Schmittgen, T. D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods25, 402–408 (2001).
doi: 10.1006/meth.2001.1262